Ceratothoa banksii ( Leach, 1818 )

Martin, Melissa B., Bruce, Niel L. & Nowak, Barbara F., 2015, Review of the fish-parasitic genus Ceratothoa Dana, 1852 (Crustacea: Isopoda: Cymothoidae) from Australia, with description of two new species, Zootaxa 3963 (3), pp. 251-294 : 254-261

Ceratothoa banksii ( Leach, 1818)

Figures 1–4

Cymothoa Banksii Leach, 1818: 353 .— Milne Edwards, 1840: 273.— Krauss, 1843: 66.— White, 1847: 110.— Ellis, 1981: 124. Cymothoa trigonocephala .— Haan, 1850: 227, figs. 7 (a–b).

Codonophilus imbricatus .— Hale, 1926: 223, figs. 15–16; 1929: 263, fig. 262.— Lanzing & O’Connor, 1975: 355, figs. 1 (a– b).— Hooper, 1983: 42.

Meinertia imbricata .— Trilles, 1973b: 1248, pl. II (10–11).

Ceratothoa imbricatus .— Brusca, 1981: 125.

Ceratothoa trigonocephalon . — Bruce, 1987: 359, figs. 12 (d–f).

Ceratothoa banksii. — Andrews, Cobcroft, Battaglene, Valdenegro, Martin & Nowak, 2013: 280.

Ceratothoa imbricata . — Hadfield, Bruce & Smit, 2014a: 26 , figs. 17, 18.

Ceratothoa cf. imbricata .— Nowak, Dawson, Basson, Deveney & Powell, 2004: 709. — Carrassón & Cribb, 2014: 173, fig. 1.

Not Cymothoa Banksi. — Gerstaecker, 1901: 259, pl. VIII, figs. 24–25 [= Ceratothoa trigonocephala ].

Excluded (identity not known)

Ceratothoa Banksii. — Schioedte & Meinert, 1883: 340, tab XIV (Cym. XXI), figs. 6–21.— Hansen, 1890: 304, tab X, fig. 4 (a– v).

Cymothoé de Banks.— Desmarest, 1825: 309.

Ceratothoa Banksii. — Heller, 1865: 148.— Filhol, 1885: 446.— Stebbing, 1893: 354.

Ceratothoa banksii. — Miers, 1876b: 105.

Meinertia Banksii. — Thielemann, 1910: 36.

Ceratothoa imbricata .— Yu & Li, 2003a: 227 –228, fig. 3.

Type and type locality. The holotype is held at The Natural History Museum, London ( BMNH.1979.402.1), presented by Leach to the then Museum of the Linnean Society and was recently figured by Hadfield et al. (2014a, figs. 17 and 18). The type locality is New Zealand, host unknown ( Hadfield et al. 2014a).

Material examined. Examined material published or identified by Hale: 1 ♀ ovig. (29 mm), 5 ♂ mature (10, 10, 12, 14, 14 mm), southeast Flinders Island, SA, 1909–1914, coll. FIS Endeavour (AM E6744).

Tasmanian material: 1 ♂ mature (24 mm), Brown River, 2 November 1953, from buccal cavity of trevally (species unknown), coll. J. R. Cunningham ( TMAG G68). 2 ♀ ovig. (22, 22 mm), 5 ♂ immature (6, 6, 12, 15, 16 mm), St. Helens, East Coast, 4 January 1963, from buccal cavity of silver trevally Pseudocaranx dentex (Bloch & Schneider, 1801) (labelled Usacaranx georgianus ) coll. B.C. Mollison ( TMAG G510). 1 ♂ mature (20 mm), Storm Bay, 20 January 1945, from buccal cavity of Gasterochisma melampus Richardson, 1845 , coll. W. Burnett ( TMAG G1793). 1 ♀ ovig. (32 mm), Bridport, December 1978, found on a bream, coll. R. J. Hardy ( TMAG G2038). 2 ♂ mature (24, 30 mm), 2 ♂ immature (14, 15 mm), from Salmon farm (SALTAS), Dover, 14 October 1987, from buccal cavity of Salmo salar Linnaeus, 1758 , coll. R. J. G. Lester (MTQ W14780). 3 ♀ pre-ovig. (20, 23, 25 mm), 4 ♂ mature (17, 18, 18, 19 mm), in TAFI sea cage, Hobart, 27 May 2008, from Latris lineata (Forster, 1801) , coll. R. Adlard (MTQ W13972).

South Australian material: 1 ♂ mature (24 mm), Second Valley, coll. A. L Campbell ( SAM C780). 1 ♀ ovig. (33 mm), 1 ♂ mature (28 mm), Port Giles, Yorke Peninsula, SA, 9 December 1975, from buccal cavity of garfish (species unknown), taken from a jetty, coll. A. F. Whitington ( SAMA C8442).

Queensland material: 9 ♀ ovig. (22, 23, 24, 24, 24, 25, 26, 26, 28 mm), 6 ♀ pre-ovig. (22, 22, 25, 25, 25, 26 mm), 2 ♂ mature (24, 27 mm), 10 ♂ immature (9, 9, 10, 10, 11, 12, 13, 13, 14, 16 mm), Moreton Bay, from Selenotoca multifasciata (Richardson, 1846) , March 1977, coll. Fisheries Branch (MTQ W7249). 1 ♂ immature (12 mm), Serpentine Creek, Brisbane, from fantail mullet Paramugil georgii (Ogilby, 1879) (as Mugil georgii ) 17 February 1975, coll. R. Harrison (MTQ W4822). 1 ♂ immature (10 mm), Great Sandy Strait, from Scatophagus argus (Linnaeus, 1766) , coll. Boult (MTQ W5747). 4 ♀ ovig. (21, 23, 24, 24 mm), 5 ♂ mature (9, 10, 12, 13, 15 mm), southeastern Queensland, year 2009, coll. T. Cribb (MTQ W31372). 1 ♀ pre-ovig. (18 mm), 1 ♂ mature (22 mm), 2 ♂ immature (7, 13 mm), Yeppoon, from buccal cavity of Selenotoca multifasciata (labelled Scatophagus multifasciatus ), coll. T. C. Marshall (MTQ W5760). 1 ♀ ovig. (24 mm), Wynnum, southeastern Queensland, 3 November 1992, coll. T. Cribb (MTQ W31373). 2 ♀ ovig. (25, 27 mm), 4 ♂ mature (9, 11, 12, 13 mm), Moreton Bay, 17 October 1979 (MTQ W31374). 1 ♀ pre-ovig. (17 mm), 3 ♂ immature (4, 5, 8 mm), Serpentine Creek, Brisbane, 14 January 1975, coll. R. Harrison (MTQ W4821). 2 ♂ mature (10, 20 mm), Moreton Bay, year 2008 (MTQ W14118). 1 ♀ ovig. (20 mm), 1 ♂ mature (19 mm), Brisbane fish market, coll. G. Johnson (MTQ W10848). 1 ♀ ovig. (34 mm), Noosa, southeastern Queensland, July 1986, from buccal cavity of Gnathanodon speciosus (Forsskål, 1775) , coll. J. Alconn (MTQ W12640). 3 ♀ pre-ovig. (10, 21, 24 mm), Great Sandy Strait, southeastern Queensland, coll. Capt. Boult (MTQ W5763).

New South Wales material: 1 ♀ ovig. (31 mm), 1 ♂ mature (13 mm), Wallaga Lakes, 19 December 1981, from buccal cavity of Pomatomus saltatrix (Linnaeus, 1766) (labelled Pomatomus saltator ), coll. C. Keenan (MTQ W10410). 5 ♀ ovig. (23, 23, 24, 24, 25 mm), 2 ♀ pre-ovig. (23, 23 mm), 2 ♂ mature (10, 13 mm), Lake Macquarie, year 1977, from buccal cavity of Girella tricuspidata (Quoy & Gaimard, 1824) , coll. C. Praegenzer (MTQ W30407). 1 ♀ ovig. (33 mm), 1 ♂ mature (19 mm), Cabarita Beach, near Bogangar, 28°20.0’S; 153°34.0’E, 3 February 1996, from buccal cavity of trevally (species unknown), coll. P. Davie (MTQ W21519). 1 ♀ pre-ovig. (32 mm), Ulladulla, April 1988, from buccal cavity of trevally (species unknown), coll. H. R. Delves (AM P38599). 1 ♀ ovig. (30 mm), 1 ♂ mature (25 mm), no location data, from buccal cavity of mullet (species unknown), presented by T. Steel (AM P9601). 1 ♀ ovig. (28 mm), north of Montague Island, 36°15.00’S, 150°14.00’E; from buccal cavity of flathead (species unknown) (AM P8828). 2 ♀ pre-ovig. (23, 22 mm), Lake Macquarie, 33°03.00’S, 151°38.00’E; year 1987, from buccal cavity of Girella tricuspidata coll. C. Praegenzer (AM P37262).

Ovigerous female. Length 27 mm, width 12 mm. Serpentine Creek, Brisbane, from buccal cavity of Selenotoca multifasicata (MTQ W7249).

Body 2.3 times as long as greatest width, dorsal surface smooth and polished in appearance, widest at pereonite 5, narrowest at pereonite 1, lateral margins weakly subparallel. Cephalon 0.4 times longer than wide, visible in dorsal view. Frontal margin apex subacute. Eyes well-developed, 0.1 times width of head. Pereonite 1 anterolateral angle with produced point; pereonite 2 posterolateral margins narrowly rounded; pereonites 5–7 dorsally arched. Coxae 2–3 posteroventral margins with prominent produced point; 4–7 with less prominent oblique carina. Pleonites 3–5 similar in width to pereonite 7; pleonite 5 with posterolateral margins overlapped by lateral margins of pleonite 4. Pleotelson 0.4 times as long as anterior width, dorsal medial surface slightly raised, lateral margins straight, posterior margin broadly truncate.

Antennula comprised of 7 articles; peduncle articles distinct and articulated; article 2 0.9 times as long as article 1; article 3 0.4 times as long as combined lengths of articles 1 and 2, 1.2 times as long as wide; extending to posterior margin of eye. Antenna comprised of 8 articles; peduncle article 3 2.6 times as long as article 2, 0.9 times as long as wide; article 4 0.9 times as long as wide, 0.6 times as long as article 3; article 5 0.3 times as long as article 4, 0.5 times as long as wide; extending to posterior margin of head. Labrum lateral margin convex, anterior margin acute.

Pereopod 1 basis 2.1 times as long as greatest width; ischium 1.8 times as long as basis; merus proximal margin with bulbous protrusion; carpus with rounded proximal margin; propodus 1.2 times as long as wide; dactylus slender, 1.8 as long as propodus, 2.1 times as long as basal width. Pereopod 2 propodus 0.9 as long as wide; dactylus 1.6 as long as propodus. Pereopod 6 basis 1.2 times as long as greatest width, ischium 1.5 times as long as basis, propodus 1.1 as long as wide, dactylus 1.3 as long as propodus. Pereopod 7 basis 1.4 times as long as greatest width; ischium 0.5 as long as basis, without protrusions; merus proximal margin with slight bulbous protrusion, merus 0.3 as long as ischium, 0.3 times as long as wide; carpus 0.2 as long as ischium, without bulbous protrusion, 0.2 times as long as wide; propodus 0.7 as long as ischium, 1 times as long as wide; dactylus slender, 1.4 as long as propodus, 2.3 times as long as basal width.

Pleopods exopod larger than endopod. Pleopod 1 exopod 2.2 times as long as wide, lateral margin strongly convex, distally broad and rounded, mesial margin strongly convex; endopod 2.7 times as long as wide, lateral margin weakly concave, distally broadly rounded, mesial margin straight, peduncle 4.2 times as wide as long, without retinaculae. Pleopods 2–5 mesial margins prominent; 3–5 endopods proximal borders do not extend beyond endopod peduncle; pleopod 1–5 with broad medial margin.

Uropod extending beyond pleotelson posterior margin, peduncle 0.6 times longer than rami, peduncle lateral margin without setae; marginal setae absent. Endopod apically slightly pointed, 4.1 times as long as greatest width, lateral margin proximally convex or distally concave, mesial margin weakly convex. Exopod extending to end of endopod, 5.9 times as long as greatest width, apically rounded, lateral margin weakly convex, terminating without setae, mesial margin weakly convex.

Male. Body 0.4 to 0.8 as long as females, lateral margins subparallel; cephalon anterior margin rounded; appendix masculina present.

Colour. Ivory white in ethanol. Other examined specimens are yellowish, orange–brown, and dark brown in ethanol.

Variation. (The variations observed are characteristics intrinsic to Ceratothoa banksii and based on all registered specimens and literature illustrations. There are no definite patterns of variation relating to host identity or region). Female: Cephalon is either subtruncate or subtriangular. Eye sizes range from 0.1 to 0.4 times the width of the cephalon posterior margin, and are circular or sub-rectangular. Body shape is rhomboid, dorsally flattened and subparallel; or broad, subtriangular and dorsally raised at pereonite 4 and 5, appearing stout and robust. The basis of pereopod 6 and pereopod 7 is either broad and convex with sharp carinae or slender with less prominent carinae. Ceratothoa banksii has a slight bulbous protrusion on the ischium of pereopods 4–7 (1 out of 30 specimens). The posterior of the pleotelson varies from subtruncate to rounded. Male: Chromatophores on dorsal body are either lightly scattered or absent.

Size. Ovigerous female: 20–34 mm (mean= 25.5 mm, N= 31), pre-ovigerous females: 10–32 mm (mean= 22.4 mm, N= 19), mature male: 14–30 mm (mean= 16.2 mm, N= 33), immature male: 5–16 mm (mean= 10.8 mm, N= 24).

Remarks. Ceratothoa banksii can be identified by the subparallel and subquadrate body shape; thickened pereonite cuticle posterior margin, with anterior portion of the pereonites noticeably darker than the posterior portion; pereonite 1 anterolateral margins with produced point, straight lateral margins of pereonites 1–4; subtruncate pleotelson posterior margin, and anterior margin similar in width or wider than pereonite 7.

Miers (1884) proposed the synonymy of Ceratothoa banksii with Ceratothoa imbricata , this later being accepted by many authors ( Stebbing 1893, Nierstrasz 1915, Trilles 1973b). Hadfield et al. (2014a, figs. 17 and 18) gave figures of the holotype of C. banksii and compared it with the holotypes of C. imbricata and Ceratothoa trigonocephala . Hadfield et al. (2014a) stated that C. banksii had a similar body shape to C. imbricata , with a larger pereonite 1, pointed anterolateral margins on pereonite 1 that extend past the eyes, and a subtriangular cephalon anterior margin, and maintained the synonymy.

The holotypes of C. banksii and C. imbricata (illustrated by Hadfield et al. 2014a) have similar body proportions, being 2.3 times longer than greatest width, with a subtriangular cephalon, broad carinae basis on pereopods 4–7, uropods extending past pleotelson and a subtruncate posterior pleotelson. Ceratothoa banksii differs from C. imbricata by the subparallel and rectangular-shaped body; pereonite 1 anterolateral projection with produced point reaching anterior region of eye (slightly extending past anterior eye margin in C. imbricata ), pereonites 1–4 lateral margins subparallel (in holotype) or becoming progressively wider (see figure 1A and 1F); pereonites lighter in colour posteriorly, gradually darker towards anterior region of pereonites; and pleotelson width similar or wider than pereonite 7. Miers (1884) noted C. imbricata was smaller, had smaller anterolateral extensions on pereonite 1 and had a slightly arched pleotelson posterior margin as compared to the holotype of C. banksii , but thought these differences to be unimportant.

Ceratothoa banksii has low host specificity, using nine host families ( Kyphosidae , Scombridae , Latridae , Carangidae , Mugilidae , Salmonidae , Scatophagidae , Pomatomidae and Hemiramphidae ). It is now known that C. imbricata has high host specificity, preferring hosts of genus Trachurus . Reports of the occurrence of C. banksii from Trachurus spp. ought to be treated with caution, as these are likely to be C. imbricata .

Ceratothoa trigonocephala ( Leach, 1818) is also similar to C. banksii , with subparallel pereonite 1–4 margins, with antennula and antenna not extending past the posterior margin of the cephalon, pereopod 7 ischium without protrusion and pereopod 7 basis with weak carina. Ceratothoa trigonocephala differs from C. banksii by the middorsal protrusion on pereonite 1, body being 2.4 times as long as greatest width, and pereonites 1 to 4 subequal in length. Schioedte & Meinert (1883) described and illustrated the cephalon of C. banksii as more blunt than the more acute cephalon of C. trigonocephala . Stebbing (1902) observed that the pereonite 1 anterior margin in C. banksii was nearly straight in comparison to that of C. trigonocephala . Bruce (1987) illustrated the brood pouch morphology of several cymothoid genera, including “ Ceratothoa trigonocephalon ” from the host Girella tricuspidata (AM P37262). Specimens from AM P37262 were examined and found to conform to the morphology of C. banksii (see variations for details).

Distribution. Present material from southeastern Queensland, South Australia, and Tasmania. Other accepted records include Schioedte & Meinert (1883), Lanzing & O’Connor (1975) and Hooper (1983) from Australia; Heller (1865), Schioedte & Meinert (1883) from Indonesia.

Hosts. Present material from the mouth of Girella tricuspidata (Kyphosidae) , Gasterochisma melampus (Scombridae) , Latris lineata (Latridae) , Salmo salar (Salmonidae) , Pseudocaranx dentex and Gnathanodon speciosus (Carangidae) , Selenotoca multifasicata and Scatophagus argus (Scatophagidae) , Pomatomus saltatrix (Pomatomidae) , Paramugil georgii and several species of mullet ( Mugilidae ), garfish ( Hemiramphidae ) and flathead ( Platycephalidae ). Two specimens (one ovigerous and one pre-ovigerous female (SAMA C8442) from Port Giles, Yorke Peninsula, were taken from a garfish and agree with the description of C. banksii given here.

Schioedte & Meinert (1883) recorded C. banksii from Diplodus cervinus hottentotus (Smith, 1844) (previously known as Sargus hottentotus Smith, 1844 ) in southern Africa. There is no evidence that C. banksii occurs in southern Africa, and that record is regarded as a misidentification ( Hadfield et al. 2014a; present study).

Figures

FIGURE 1. Ceratothoa banksii, ovigerous females (25, 23 mm; MTQ W 30407 A – E) (27 mm; MTQ W 7249 F, G). A, dorsal view of females; B, drosal view of pereonite 1 and cephalon; C, antennula; D, antenna; E, lateral view; F, dorsal view; G, lateral view.

FIGURE 2. Ceratothoa banksii, immature males (10, 13 mm) (MTQ W 30407). A, ventral view of female mouthparts; B, dorsal view of pleotelson; C, dorsal view of males; D, uropod; E, ventral view of pleotelson.

FIGURE 3. Ceratothoa banksii, ovigerous female (23 mm) (MTQ W 30407). A, mandible; B, maxillula tip; C, maxilliped; D, maxilla.

FIGURE 4. Ceratothoa banksii, ovigerous female (25 mm) (MTQ W 30407). A – D, pereopods 1, 2, 6, 7 respectively; E – I, pleopods 1 – 5 respectively.